Báo cáo y học: "Bilateral olfaction: two is better than one for navigation" pdf

A recent study reveals that fruit fly larvae can localize odor sources using unilateral inputs from a single functional sensory neuron, but that an enhanced signal-to-noise ratio provide

Genome BBiiooggyy 2008, 99::212

Addresses: *National Institute of Child Health and Human Development, NIH, Lincoln Drive, Bethesda, MD 20892, USA

†National Institute of Standards and Technology, Gaithersburg, MD 20899, USA

Correspondence: Mark Stopfer Email: stopferm@mail.nih.gov

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Do animals require bilateral input to track odors? A recent study reveals that fruit fly larvae can

localize odor sources using unilateral inputs from a single functional sensory neuron, but that an

enhanced signal-to-noise ratio provided by dual inputs is helpful in more challenging environments

Published: 31 March 2008

Genome BBiioollooggyy 2008, 99::212 (doi:10.1186/gb-2008-9-3-212)

The electronic version of this article is the complete one and can be

found online at http://genomebiology.com/2008/9/3/212

© 2008 BioMed Central Ltd

Biological sensory systems often make use of asymmetries in

sensory inputs to extract information about the environment

The visual system, for example, exploits disparities in the

two-dimensional images obtained from the left and the right

eyes to extract information about depth [1] The auditory

system uses the phase and intensity differences of stereo

inputs to localize sound sources [2] Relatively little is known

about the importance of bilateral inputs in olfaction Our own

noses feature twin nostrils; insects have paired antennae

What advantages do such configurations provide? A recent

study by Louis and colleagues [3] examined the significance

of paired inputs for odor navigation in an animal offering

numerous experimental advantages, the larva of the fruit fly,

Drosophila melanogaster

Studying how animals carry out chemotaxis, that is, how

they navigate through chemical gradients, requires careful

behavioral assays conducted within well-controlled spatial

distributions of chemicals In the case of olfaction, it is a

significant technical challenge to generate the stable odor

gradients needed for such a study Louis et al [3] developed

a novel and clever approach: they built a small test chamber

whose ceiling, an inverted 96-well plate, suspended an

ordered array of droplets of sequentially diluted odorants

(Figure 1) The authors confirmed that this array generated

the desired airborne odor gradient within the test chamber

by means of Fourier transformed infrared spectroscopy

Equipped with this well-controlled stimulus field, the

authors set about examining chemotaxis in fruit fly larvae

In the larva, the transduction of chemical stimuli into neural representations begins in two dorsally located olfactory organs that are about 100 micrometers apart Each olfactory organ normally contains 21 sensory neurons, each expressing one or two receptor genes together with the universally coexpressed OR83b gene [4] Earlier studies by the authors had established that knocking out the OR83b co-receptor gene removes essentially all odor-driven behavior

in these larvae [4] By randomly rescuing the co-receptor gene in either the left or the right olfactory organ in transgenic OR83b knockout preparations, the authors generated unilateral animals - perfect for answering interesting questions about bilateral chemoreception

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Do the larvae require a full complement of receptors to reliably locate odor sources? Surprisingly, transgenic larvae with unilateral input from a single olfactory neuron were able to locate odor sources just as well as wild-type larvae

In fact, bilateral transgenic larvae with a single functional receptor neuron in each of their olfactory organs actually showed greater odor sensitivity than wild-type larvae This apparently odd result may point toward an odor-coding scheme in the wild type in which ensembles of sensors with

a low signal-to-noise ratio are combined with inputs with a high signal-to-noise ratio Or, alternatively, in the wild type, competition among downstream neurons driven by different receptor neurons could diminish overall

sensitivity Schemes like these may function to promote

odor discrimination, another task mediated by the same

circuitry

The authors found that both transgenic and wild-type larvae

navigate by constantly orienting themselves along the

direction of the steepest local concentration gradient (Figure 1)

The larval rate of turning was greatest in low-concentration

regions and decreased as the larvae progressed towards the

concentration peak This ‘direct chemotaxis’ is strikingly

different from the ‘biased random walk’ strategy used by

bacteria, which change direction at random, but alter the

intervals between turns to bias movement toward attractants

and away from repellants [5]

Interestingly, the authors noticed a side-dependent bias in

the unilateral animals Both left- and right-sided animals

have a single functional receptor neuron, yet right-sided

larvae performed chemotaxis significantly better than their

left-sided counterparts In larvae (unlike in adult flies)

sensory inputs from each side remain segregated

throughout the peripheral olfactory pathway Thus, the

observed right-side bias suggests disparities in downstream processing This inherent right-side bias is not unique to these larvae - lateralization of olfactory processing has also been reported in a few other invertebrate species [6] The importance of this bias for odor processing and olfactory behavior remains unclear

The two olfactory organs are so close together in fruit fly larvae that any odor concentration differences between them would be undetectably slight, and so it seems unlikely that bilateral concentration comparisons could provide useful cues for successful navigation So how do these organisms locate odor sources? The most likely possibility

is that the larvae use a mechanism that allows comparisons between at least two consecutive concentration measurements made over time Thus, the results from Louis

et al [3] suggest that a form of working memory of the concentration of recent samples is required for chemotaxis

by Drosophila larvae

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Why then have two separate olfactory organs? The authors found that fruit fly larvae with dual inputs performed significantly better than their unilateral counterparts when challenged to navigate through complex odor environments with shallow, linear gradients and high offset concen-trations How do bilateral inputs aid with chemotaxis? It was not the case that simply doubling olfactory input lowered olfactory response thresholds, as the lowest concentration in the behavioral assay was above the detection level of the unilateral animals Louis et al [3] note that, theoretically, integrating information from n redundant sensors can result

in √n times enhancement in the signal-to-noise ratio, provided the noise in the separate sensors remains uncorrelated Hence, the bilateral larvae should possess a lower detection level and an ability to make concentration measurements with a resolution at most √2 times better than the unilateral animals (Figure 2) Perhaps two physically separated olfactory organs provide inputs that are less noise-correlated than inputs from a single receptor organ The observed improvement in performance may be due to an improved signal-to-noise ratio provided by the neural integration of redundant sensory information, or to a nonlinear process of lateralized bilateral inputs in the central brain, or to both

Adult flies may use a different strategy Unlike larvae, in adults around 10-40 receptor neurons of the same type are present in each antenna and project bilaterally to both left and right antennal lobes Hence, in the adult, integration

of redundant inputs begins at a very early stage in olfactory processing Whether this unique wiring scheme enhances the spatial comparison of simultaneous bilateral inputs [7]

or only increases the number of redundant receptors and, therefore, the signal-to-noise ratio, remains unknown

Genome BBiioollooggyy 2008, 99::212

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Fiigguurree 11

Investigating chemotaxis byDrosophila larvae ((aa)) Louis et al [3]

generated a well-structured airborne odor concentration gradient by

suspending droplets of odorant at different concentrations from the

ceiling of their test chamber (yellow denotes the highest concentration;

black the lowest) The arrangement of droplets generated a spatial

concentration distribution that varies from one end of the chamber to

the other and from the middle of the chamber (high) to the sides ((bb))

Both unilateral and bilateral transgenic larvae navigate odor fields by

detecting local concentration gradients By moving along the direction of

the steepest intensity variation, the larvae reliably locate the source of

the odor

max

Chamber for behavioral tests

Odor concentration

Chemotaxing larvae ascend along odor gradients

Odor

concentration

Suspended droplets

of diluted odorant

(a)

(b)

Navigation path

Navigation path

Stereo olfactory cues are more important for humans and

other animals with olfactory organs that are well separated

in space [8,9] Humans, for example, can track odors based

on comparisons of concentration measurements made over

time alone, but also use inter-nostril concentration

differ-ences to improve tracking performance: occluding one nostril

or providing the same odor information to both nostrils

significantly reduces a person’s ability to locate odor sources

quickly [9]

As shown by Louis and colleagues [3], Drosophila, with its

simple brain structure and wealth of genetic tools, provides a

useful system for the study of olfaction and odor-evoked

behavior It will be interesting to determine the role of

bilateral inputs in adult flies and compare their navigation

strategies with those of the larvae And it will be especially interesting to explore the significance and neural basis of the transient, working memory processes apparently needed to mediate chemotaxis The use of genetically manipulated flies and their larvae will no doubt contribute greatly to these efforts [10]

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Fiigguurree 22

Neural integration of bilateral olfactory inputs enhances signal-to-noise ratio ((aa)) Schematic diagram of the bilateral olfactory input pathways and a

hypothetical central neuron (grey circle) receiving those inputs Information is transmitted as spiking activity Typically, in the absence of any olfactory

stimulus, the receptor neurons tend to show a baseline spiking response that contributes to the ‘noise’ in the system Both the detection level and the measurement resolution of the system are dependent on the input noise level ((bb)) Neural integration can reduce uncorrelated noise The plots on the

left represent the firing rate of two receptor neurons over time The baseline fluctuations observed in the two independent channels (left) are reduced after integrating them (right), thus improving signal-to-noise ratio This improvement may be the chief contribution of dual olfactory inputs to

chemotaxis The green box indicates the release of a puff of odor

central location

From left

From right

Neural integration

Less noise

Improved signal-to-noise ratio Odor response

Input spikes

Output spikes

Noise

Time

Time

(a)

(b)

Time

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